Chapter

5 Mineral Nutrition

MINERAL NUTRIENTS ARE ELEMENTS acquired primarily in the

form of inorganic ions from the soil. Although mineral nutrients continu-
ally cycle through all organisms, they enter the biosphere predominantly
through the root systems of plants, so in a sense plants act as the “miners”
of Earth’s crust (Epstein 1999). The large surface area of roots and their
ability to absorb inorganic ions at low concentrations from the soil solu-
tion make mineral absorption by plants a very effective process. After
being absorbed by the roots, the mineral elements are translocated to the
various parts of the plant, where they are utilized in numerous biological
functions. Other organisms, such as mycorrhizal fungi and nitrogen-fix-
ing bacteria, often participate with roots in the acquisition of nutrients.
The study of how plants obtain and use mineral nutrients is called
mineral nutrition. This area of research is central to modern agriculture
and environmental protection. High agricultural yields depend strongly
on fertilization with mineral nutrients. In fact, yields of most crop plants
increase linearly with the amount of fertilizer that they absorb (Loomis
and Conner 1992). To meet increased demand for food, world con-
sumption of the primary fertilizer mineral elements—nitrogen, phos-
phorus, and potassium—rose steadily from 112 million metric tons in
1980 to 143 million metric tons in 1990 and has remained constant
through the last decade.
Crop plants, however, typically use less than half of the fertilizer
applied (Loomis and Conner 1992). The remaining minerals may leach
into surface waters or groundwater, become attached to soil particles, or
contribute to air pollution. As a consequence of fertilizer leaching, many
water wells in the United States no longer meet federal standards for
nitrate concentrations in drinking water (Nolan and Stoner 2000). On a
brighter note, plants are the traditional means for recycling animal
wastes and are proving useful for removing deleterious minerals from
toxic-waste dumps (Macek et al. 2000). Because of the complex nature
of plant–soil–atmosphere relationships, studies in the area of mineral
nutrition involve atmospheric chemists, soil scientists, hydrologists,
microbiologists, and ecologists, as well as plant physiologists.
68 Chapter 5

In this chapter we will discuss first the nutritional needs bon) compounds of the plant. Plants assimilate these
of plants, the symptoms of specific nutritional deficiencies, nutrients via biochemical reactions involving oxida-
and the use of fertilizers to ensure proper plant nutrition. tion and reduction.
Then we will examine how soil and root structure influence 2. The second group is important in energy storage
the transfer of inorganic nutrients from the environment reactions or in maintaining structural integrity.
into a plant. Finally, we will introduce the topic of mycor- Elements in this group are often present in plant tis-
rhizal associations. Chapters 6 and 12 address additional sues as phosphate, borate, and silicate esters in which
aspects of solute transport and nutrient assimilation, the elemental group is bound to the hydroxyl group
respectively. of an organic molecule (i.e., sugar–phosphate).
3. The third group is present in plant tissue as either
ESSENTIAL NUTRIENTS, DEFICIENCIES, free ions or ions bound to substances such as the pec-
AND PLANT DISORDERS tic acids present in the plant cell wall. Of particular
importance are their roles as enzyme cofactors and in
Only certain elements have been determined to be essen- the regulation of osmotic potentials.
tial for plant growth. An essential element is defined as
one whose absence prevents a plant from completing its 4. The fourth group has important roles in reactions
involving electron transfer.
life cycle (Arnon and Stout 1939) or one that has a clear
physiological role (Epstein 1999). If plants are given these Naturally occurring elements, other than those listed in
essential elements, as well as energy from sunlight, they Table 5.1, can also accumulate in plant tissues. For exam-
can synthesize all the compounds they need for normal ple, aluminum is not considered to be an essential element,
growth. Table 5.1 lists the elements that are considered to but plants commonly contain from 0.1 to 500 ppm alu-
be essential for most, if not all, higher plants. The first three minum, and addition of low levels of aluminum to a nutri-
elements—hydrogen, carbon, and oxygen—are not con- ent solution may stimulate plant growth (Marschner 1995).
sidered mineral nutrients because
they are obtained primarily from
TABLE 5.1
water or carbon dioxide. Adequate tissue levels of elements that may be required by plants
Essential mineral elements are
usually classified as macronutrients Concentration Relative number of
or micronutrients, according to Chemical in dry matter atoms with respect
Element symbol (% or ppm)a to molybdenum
their relative concentration in plant
tissue. In some cases, the differ- Obtained from water or carbon dioxide
ences in tissue content of macronu- Hydrogen H 6 60,000,000
Carbon C 45 40,000,000
trients and micronutrients are not
Oxygen O 45 30,000,000
as great as those indicated in Table
5.1. For example, some plant tis- Obtained from the soil
sues, such as the leaf mesophyll, Macronutrients
have almost as much iron or man- Nitrogen N 1.5 1,000,000
ganese as they do sulfur or magne- Potassium K 1.0 250,000
sium. Many elements often are pre- Calcium Ca 0.5 125,000
sent in concentrations greater than Magnesium Mg 0.2 80,000
the plant’s minimum requirements. Phosphorus P 0.2 60,000
Some researchers have argued Sulfur S 0.1 30,000
Silicon Si 0.1 30,000
that a classification into macro-
nutrients and micronutrients is Micronutrients
difficult to justify physiologically. Chlorine Cl 100 3,000
Mengel and Kirkby (1987) have Iron Fe 100 2,000
proposed that the essential ele- Boron B 20 2,000
Manganese Mn 50 1,000
ments be classified instead accord-
Sodium Na 10 400
ing to their biochemical role and
Zinc Zn 20 300
physiological function. Table 5.2 Copper Cu 6 100
shows such a classification, in Nickel Ni 0.1 2
which plant nutrients have been Molybdenum Mo 0.1 1
divided into four basic groups:
Source: Epstein 1972, 1999.
1. The first group of essential ele- a The values for the nonmineral elements (H, C, O) and the macronutrients are percentages. The
ments forms the organic (car- values for micronutrients are expressed in parts per million.
 Mineral Nutrition 69

TABLE 5.2
Classification of plant mineral nutrients according to biochemical function
Mineral nutrient Functions
Group 1 Nutrients that are part of carbon compounds
N Constituent of amino acids, amides, proteins, nucleic acids, nucleotides, coenzymes, hexoamines, etc.
S Component of cysteine, cystine, methionine, and proteins. Constituent of lipoic acid, coenzyme A, thiamine
pyrophosphate, glutathione, biotin, adenosine-5′-phosphosulfate, and 3-phosphoadenosine.
Group 2 Nutrients that are important in energy storage or structural integrity
P Component of sugar phosphates, nucleic acids, nucleotides, coenzymes, phospholipids, phytic acid, etc. Has a
key role in reactions that involve ATP.
Si Deposited as amorphous silica in cell walls. Contributes to cell wall mechanical properties, including rigidity
and elasticity.
B Complexes with mannitol, mannan, polymannuronic acid, and other constituents of cell walls. Involved in cell
elongation and nucleic acid metabolism.
Group 3 Nutrients that remain in ionic form
K Required as a cofactor for more than 40 enzymes. Principal cation in establishing cell turgor and maintaining
cell electroneutrality.
Ca Constituent of the middle lamella of cell walls. Required as a cofactor by some enzymes involved in the
hydrolysis of ATP and phospholipids. Acts as a second messenger in metabolic regulation.
Mg Required by many enzymes involved in phosphate transfer. Constituent of the chlorophyll molecule.
Cl Required for the photosynthetic reactions involved in O2 evolution.
Mn Required for activity of some dehydrogenases, decarboxylases, kinases, oxidases, and peroxidases. Involved
with other cation-activated enzymes and photosynthetic O2 evolution.
Na Involved with the regeneration of phosphoenolpyruvate in C4 and CAM plants. Substitutes for potassium in
some functions.
Group 4 Nutrients that are involved in redox reactions
Fe Constituent of cytochromes and nonheme iron proteins involved in photosynthesis, N2 fixation, and respiration.
Zn Constituent of alcohol dehydrogenase, glutamic dehydrogenase, carbonic anhydrase, etc.
Cu Component of ascorbic acid oxidase, tyrosinase, monoamine oxidase, uricase, cytochrome oxidase, phenolase,
laccase, and plastocyanin.
Ni Constituent of urease. In N2-fixing bacteria, constituent of hydrogenases.
Mo Constituent of nitrogenase, nitrate reductase, and xanthine dehydrogenase.

Source: After Evans and Sorger 1966 and Mengel and Kirkby 1987.

Many species in the genera Astragalus, Xylorhiza, and Stan- a complex medium such as soil. In the nineteenth century,
leya accumulate selenium, although plants have not been several researchers, including Nicolas-Théodore de Saus-
shown to have a specific requirement for this element. sure, Julius von Sachs, Jean-Baptiste-Joseph-Dieudonné
Cobalt is part of cobalamin (vitamin B12 and its deriva- Boussingault, and Wilhelm Knop, approached this problem
tives), a component of several enzymes in nitrogen-fixing by growing plants with their roots immersed in a nutrient
microorganisms. Thus cobalt deficiency blocks the devel- solution containing only inorganic salts. Their demonstra-
opment and function of nitrogen-fixing nodules. Nonethe- tion that plants could grow normally with no soil or organic
less, plants that do not fix nitrogen, as well as nitrogen-fix- matter proved unequivocally that plants can fulfill all their
ing plants that are supplied with ammonium or nitrate, do needs from only inorganic elements and sunlight.
not require cobalt. Crop plants normally contain only rela- The technique of growing plants with their roots
tively small amounts of nonessential elements. immersed in nutrient solution without soil is called solu-
tion culture or hydroponics (Gericke 1937). Successful
Special Techniques Are Used in Nutritional Studies hydroponic culture (Figure 5.1A) requires a large volume
To demonstrate that an element is essential requires that of nutrient solution or frequent adjustment of the nutrient
plants be grown under experimental conditions in which solution to prevent nutrient uptake by roots from produc-
only the element under investigation is absent. Such condi- ing radical changes in nutrient concentrations and pH of
tions are extremely difficult to achieve with plants grown in the medium. A sufficient supply of oxygen to the root sys-
70 Chapter 5

(A) Hydroponic growth system ponic culture, plants are grown in a

supporting material such as sand,
Plant gravel, vermiculite, or expanded
support clay (i.e., kitty litter). Nutrient solu-
system tions are then flushed through the
Air supporting material, and old solu-
tions are removed by leaching. In
Nutrient another form of hydroponic culture,
solution plant roots lie on the surface of a
Air bubbles
trough, and nutrient solutions flow
in a thin layer along the trough over
the roots (Cooper 1979, Asher and
(B) Nutrient film growth system Edwards 1983). This nutrient film
Nutrient solution growth system ensures that the
roots receive an ample supply of
oxygen (Figure 5.1B).
Nutrient Another alternative, which has
recovery
chamber sometimes been heralded as the
medium of the future, is to grow the
plants aeroponically (Weathers and
Zobel 1992). In this technique, plants
are grown with their roots sus-
pended in air while being sprayed
Pump continuously with a nutrient solu-
tion (Figure 5.1C). This approach
(C) Aeroponic growth system provides easy manipulation of the
gaseous environment around the
root, but it requires higher levels of
Nutrient nutrients than hydroponic culture
mist Plant holdings
chamber cover seals chamber does to sustain rapid plant growth.
For this reason and other technical
difficulties, the use of aeroponics is
not widespread.

Nutrient Solutions Can

Sustain Rapid Plant Growth
Nutrient
solution Motor-driven rotor Over the years, many formulations
generates mist have been used for nutrient solu-
tions. Early formulations developed
FIGURE 5.1 Hydroponic and aeroponic systems for growing plants in nutrient solu- by Knop in Germany included only
tions in which composition and pH can be automatically controlled. (A) In a hydro- KNO3, Ca(NO3)2, KH2PO4, MgSO4,
ponic system, the roots are immersed in the nutrient solution, and air is bubbled and an iron salt. At the time this
through the solution. (B) An alternative hydroponic system, often used in commer- nutrient solution was believed to
cial production, is the nutrient film growth system, in which the nutrient solution is contain all the minerals required by
pumped as a thin film down a shallow trough surrounding the plant roots. In this
system the composition and pH of the nutrient solution can be controlled automati- the plant, but these experiments
cally. (C) In the aeroponic system, the roots are suspended over the nutrient solu- were carried out with chemicals that
tion, which is whipped into a mist by a motor-driven rotor. (C after Weathers and were contaminated with other ele-
Zobel 1992.) ments that are now known to be
essential (such as boron or molyb-
denum). Table 5.3 shows a more
modern formulation for a nutrient
tem—also critical—may be achieved by vigorous bubbling solution. This formulation is called a modified Hoagland
of air through the medium. solution, named after Dennis R. Hoagland, a researcher who
Hydroponics is used in the commercial production of was prominent in the development of modern mineral nutri-
many greenhouse crops. In one form of commercial hydro- tion research in the United States.
 Mineral Nutrition 71

TABLE 5.3
Composition of a modified Hoagland nutrient solution for growing plants
Concentration Concentration Volume of stock Final
Molecular of stock of stock solution per liter concentration
Compound weight solution solution of final solution Element of element

g mol–1 mM g L–1 mL mM ppm

Macronutrients
KNO3 101.10 1,000 101.10 6.0 N 16,000 224
Ca(NO3)2⋅ 4H2O 236.16 1,000 236.16 4.0 K 6,000 235
NH4H2PO4 115.08 1,000 115.08 2.0 Ca 4,000 160
MgSO4⋅7H2O 246.48 1,000 246.49 1.0 P 2,000 62
S 1,000 32
Mg 1,000 24
Micronutrients
KCl 74.55 25 1.864 Cl 50 1.77
H3BO3 61.83 12.5 0.773 B 25 0.27
MnSO4⋅H2O 169.01 1.0 0.169 Mn 2.0 0.11
2.0
ZnSO4⋅7H2O 287.54 1.0 0.288 Zn 2.0 0.13
CuSO4⋅5H2O 249.68 0.25 0.062 Cu 0.5 0.03
H2MoO4 (85% MoO3) 161.97 0.25 0.040 Mo 0.5 0.05
NaFeDTPA (10% Fe) 468.20 64 30.0 0.3–1.0 Fe 16.1–53.7 1.00–3.00
Optionala
NiSO4⋅6H2O 262.86 0.25 0.066 2.0 Ni 0.5 0.03
Na2SiO3⋅9H2O 284.20 1,000 284.20 1.0 Si 1,000 28
Source: After Epstein 1972.
Note: The macronutrients are added separately from stock solutions to prevent precipitation during preparation of the nutrient solution. A com-
bined stock solution is made up containing all micronutrients except iron. Iron is added as sodium ferric diethylenetriaminepentaacetate
(NaFeDTPA, trade name Ciba-Geigy Sequestrene 330 Fe; see Figure 5.2); some plants, such as maize, require the higher level of iron shown in the
table.
a Nickel is usually present as a contaminant of the other chemicals, so it may not need to be added explicitly. Silicon, if included, should be added
first and the pH adjusted with HCl to prevent precipitation of the other nutrients.

A modified Hoagland solution contains all of the known in the pH of the medium that is commonly observed when
mineral elements needed for rapid plant growth. The con- the nitrogen is supplied solely as nitrate anion (Asher and
centrations of these elements are set at the highest possible Edwards 1983). Even when the pH of the medium is kept
levels without producing toxicity symptoms or salinity stress neutral, most plants grow better if they have access to both
and thus may be several orders of magnitude higher than NH4+ and NO3– because absorption and assimilation of the
those found in the soil around plant roots. For example, two nitrogen forms promotes cation–anion balance within
whereas phosphorus is present in the soil solution at con- the plant (Raven and Smith 1976; Bloom 1994).
centrations normally less than 0.06 ppm, here it is offered at A significant problem with nutrient solutions is main-
62 ppm (Epstein 1972). Such high initial levels permit plants taining the availability of iron. When supplied as an inor-
to be grown in a medium for extended periods without ganic salt such as FeSO4 or Fe(NO3)2, iron can precipitate
replenishment of the nutrients. Many researchers, however, out of solution as iron hydroxide. If phosphate salts are
dilute their nutrient solutions severalfold and replenish them present, insoluble iron phosphate will also form. Precipi-
frequently to minimize fluctuations of nutrient concentra- tation of the iron out of solution makes it physically
tion in the medium and in plant tissue. unavailable to the plant, unless iron salts are added at fre-
Another important property of the modified Hoagland quent intervals. Earlier researchers approached this prob-
formulation is that nitrogen is supplied as both ammonium lem by adding iron together with citric acid or tartaric acid.
(NH4+) and nitrate (NO3–). Supplying nitrogen in a balanced Compounds such as these are called chelators because they
mixture of cations and anions tends to reduce the rapid rise form soluble complexes with cations such as iron and cal-
72 Chapter 5

cium in which the cation is held by ionic forces, rather than • Both chronic and acute deficiencies of several ele-
by covalent bonds. Chelated cations thus are physically ments may occur simultaneously.
more available to a plant. • Deficiencies or excessive amounts of one element
More modern nutrient solutions use the chemicals eth- may induce deficiencies or excessive accumulations
ylenediaminetetraacetic acid (EDTA) or diethylenetri- of another.
aminepentaacetic acid (DTPA, or pentetic acid) as chelat-
ing agents (Sievers and Bailar 1962). Figure 5.2 shows the • Some virus-induced plant diseases may produce
symptoms similar to those of nutrient deficiencies.
structure of DTPA. The fate of the chelation complex dur-
ing iron uptake by the root cells is not clear; iron may be Nutrient deficiency symptoms in a plant are the expres-
released from the chelator when it is reduced from Fe3+ to sion of metabolic disorders resulting from the insufficient
Fe2+ at the root surface. The chelator may then diffuse back supply of an essential element. These disorders are related
into the nutrient (or soil) solution and react with another to the roles played by essential elements in normal plant
Fe3+ ion or other metal ions. After uptake, iron is kept sol- metabolism and function. Table 5.2 lists some of the roles
uble by chelation with organic compounds present in plant of essential elements.
cells. Citric acid may play a major role in iron chelation and Even though each essential element participates in many
its long-distance transport in the xylem. different metabolic reactions, some general statements
about the functions of essential elements in plant metabo-
Mineral Deficiencies Disrupt Plant Metabolism lism are possible. In general, the essential elements function
and Function in plant structure, metabolic function, and osmoregulation
Inadequate supply of an essential element results in a of plant cells. More specific roles may be related to the abil-
nutritional disorder manifested by characteristic deficiency ity of divalent cations such as calcium or magnesium to
symptoms. In hydroponic culture, withholding of an essen- modify the permeability of plant membranes. In addition,
tial element can be readily correlated with a given set of research continues to reveal specific roles of these elements
symptoms for acute deficiencies. Diagnosis of soil-grown in plant metabolism; for example, calcium acts as a signal
plants can be more complex, for the following reasons: to regulate key enzymes in the cytosol (Hepler and Wayne
1985; Sanders et al. 1999). Thus, most essential elements
have multiple roles in plant metabolism.
When relating acute deficiency symptoms to a particu-
O
lar essential element, an important clue is the extent to
(A) O
O which an element can be recycled from older to younger
–
O C CH2 CH2 C O– leaves. Some elements, such as nitrogen, phosphorus, and
CH2 C O–
O potassium, can readily move from leaf to leaf; others, such
NCH2CH2NCH2CH2N O
–
O C CH2 as boron, iron, and calcium, are relatively immobile in most
CH2 C O–
plant species (Table 5.4). If an essential element is mobile,
O
deficiency symptoms tend to appear first in older leaves.
(B)
Deficiency of an immobile essential element will become
C O–
evident first in younger leaves. Although the precise mech-
CH2 anisms of nutrient mobilization are not well understood,
CH2CH2 CH2CH2
O O
N
–
O C CH2 N Fe3+ N CH2 C O–
TABLE 5.4
O– CH2 Mineral elements classified on the basis of their
CH2 C mobility within a plant and their tendency to
O retranslocate during deficiencies
C O–
Mobile Immobile
O
Nitrogen Calcium
FIGURE 5.2 Chemical structure of the chelator DTPA by Potassium Sulfur
itself (A) and chelated to an Fe3+ ion (B). Iron binds to Magnesium Iron
DTPA through interaction with three nitrogen atoms and Phosphorus Boron
the three ionized oxygen atoms of the carboxylate groups Chlorine Copper
(Sievers and Bailar 1962). The resulting ring structure Sodium
clamps the metallic ion and effectively neutralizes its reac-
Zinc
tivity in solution. During the uptake of iron at the root sur-
face, Fe3+ appears to be reduced to Fe2+, which is released Molybdenum
from the DTPA–iron complex. The chelator can then bind to Note: Elements are listed in the order of their abundance in the
other available Fe3+ ions. plant.
 Mineral Nutrition 73

plant hormones such as cytokinins appear to be involved occur simultaneously in all leaves or even initially in the
(see Chapter 21). In the discussion that follows, we will older leaves.
describe the specific deficiency symptoms and functional
roles for the mineral essential elements as they are grouped Group 2: Deficiencies in mineral nutrients that are impor-
in Table 5.2. tant in energy storage or structural integrity. This group
consists of phosphorus, silicon, and boron. Phosphorus and
Group 1: Deficiencies in mineral nutrients that are part silicon are found at concentrations within plant tissue that
of carbon compounds. This first group consists of nitro- warrant their classification as macronutrients, whereas
gen and sulfur. Nitrogen availability in soils limits plant boron is much less abundant and considered a micronutri-
productivity in most natural and agricultural ecosystems. ent. These elements are usually present in plants as ester
By contrast, soils generally contain sulfur in excess. linkages to a carbon molecule.
Nonetheless, nitrogen and sulfur share the property that
their oxidation–reduction states range widely (see Chapter PHOSPHORUS. Phosphorus (as phosphate, PO43–) is an inte-
12). Some of the most energy-intensive reactions in life con- gral component of important compounds of plant cells,
vert the highly oxidized, inorganic forms absorbed from including the sugar–phosphate intermediates of respiration
the soil into the highly reduced forms found in organic and photosynthesis, and the phospholipids that make up
compounds such as amino acids. plant membranes. It is also a component of nucleotides
used in plant energy metabolism (such as ATP) and in
NITROGEN. Nitrogen is the mineral element that plants DNA and RNA. Characteristic symptoms of phosphorus
require in greatest amounts. It serves as a constituent of deficiency include stunted growth in young plants and a
many plant cell components, including amino acids and dark green coloration of the leaves, which may be mal-
nucleic acids. Therefore, nitrogen deficiency rapidly inhibits formed and contain small spots of dead tissue called
plant growth. If such a deficiency persists, most species necrotic spots (for a picture, see Web Topic 5.1).
show chlorosis (yellowing of the leaves), especially in the As in nitrogen deficiency, some species may produce
older leaves near the base of the plant (for pictures of nitro- excess anthocyanins, giving the leaves a slight purple col-
gen deficiency and the other mineral deficiencies described oration. In contrast to nitrogen deficiency, the purple col-
in this chapter, see Web Topic 5.1). Under severe nitrogen oration of phosphorus deficiency is not associated with
deficiency, these leaves become completely yellow (or tan) chlorosis. In fact, the leaves may be a dark greenish purple.
and fall off the plant. Younger leaves may not show these Additional symptoms of phosphorus deficiency include
symptoms initially because nitrogen can be mobilized from the production of slender (but not woody) stems and the
older leaves. Thus a nitrogen-deficient plant may have light death of older leaves. Maturation of the plant may also be
green upper leaves and yellow or tan lower leaves. delayed.
When nitrogen deficiency develops slowly, plants may
have markedly slender and often woody stems. This wood- SILICON. Only members of the family Equisetaceae—called
iness may be due to a buildup of excess carbohydrates that scouring rushes because at one time their ash, rich in gritty
cannot be used in the synthesis of amino acids or other silica, was used to scour pots—require silicon to complete
nitrogen compounds. Carbohydrates not used in nitrogen their life cycle. Nonetheless, many other species accumu-
metabolism may also be used in anthocyanin synthesis, late substantial amounts of silicon within their tissues and
leading to accumulation of that pigment. This condition is show enhanced growth and fertility when supplied with
revealed as a purple coloration in leaves, petioles, and adequate amounts of silicon (Epstein 1999).
stems of some nitrogen-deficient plants, such as tomato Plants deficient in silicon are more susceptible to lodg-
and certain varieties of corn. ing (falling over) and fungal infection. Silicon is deposited
primarily in the endoplasmic reticulum, cell walls, and
SULFUR. Sulfur is found in two amino acids and is a con- intercellular spaces as hydrated, amorphous silica
stituent of several coenzymes and vitamins essential for (SiO2·nH2O). It also forms complexes with polyphenols and
metabolism. Many of the symptoms of sulfur deficiency are thus serves as an alternative to lignin in the reinforcement
similar to those of nitrogen deficiency, including chlorosis, of cell walls. In addition, silicon can ameliorate the toxicity
stunting of growth, and anthocyanin accumulation. This of many heavy metals.
similarity is not surprising, since sulfur and nitrogen are
both constituents of proteins. However, the chlorosis BORON. Although the precise function of boron in plant
caused by sulfur deficiency generally arises initially in metabolism is unclear, evidence suggests that it plays roles
mature and young leaves, rather than in the old leaves as in cell elongation, nucleic acid synthesis, hormone
in nitrogen deficiency, because unlike nitrogen, sulfur is not responses, and membrane function (Shelp 1993). Boron-
easily remobilized to the younger leaves in most species. deficient plants may exhibit a wide variety of symptoms,
Nonetheless, in many plant species sulfur chlorosis may depending on the species and the age of the plant.
74 Chapter 5

A characteristic symptom is black necrosis of the young be preceded by a general chlorosis and downward hook-
leaves and terminal buds. The necrosis of the young leaves ing of the young leaves. Young leaves may also appear
occurs primarily at the base of the leaf blade. Stems may be deformed. The root system of a calcium-deficient plant
unusually stiff and brittle. Apical dominance may also be may appear brownish, short, and highly branched. Severe
lost, causing the plant to become highly branched; how- stunting may result if the meristematic regions of the plant
ever, the terminal apices of the branches soon become die prematurely.
necrotic because of inhibition of cell division. Structures
such as the fruit, fleshy roots, and tubers may exhibit necro- MAGNESIUM. In plant cells, magnesium ions (Mg2+) have a
sis or abnormalities related to the breakdown of internal specific role in the activation of enzymes involved in respi-
tissues. ration, photosynthesis, and the synthesis of DNA and RNA.
Magnesium is also a part of the ring structure of the chloro-
Group 3: Deficiencies in mineral nutrients that remain phyll molecule (see Figure 7.6A). A characteristic symptom
in ionic form. This group includes some of the most of magnesium deficiency is chlorosis between the leaf veins,
familiar mineral elements: The macronutrients potassium, occurring first in the older leaves because of the mobility of
calcium, and magnesium, and the micronutrients chlorine, this element. This pattern of chlorosis results because the
manganese, and sodium. They may be found in solution in chlorophyll in the vascular bundles remains unaffected for
the cytosol or vacuoles, or they may be bound electrostati- longer periods than the chlorophyll in the cells between the
cally or as ligands to larger carbon-containing compounds. bundles does. If the deficiency is extensive, the leaves may
become yellow or white. An additional symptom of mag-
POTASSIUM. Potassium, present within plants as the cation nesium deficiency may be premature leaf abscission.
K+, plays an important role in regulation of the osmotic
potential of plant cells (see Chapters 3 and 6). It also acti- CHLORINE. The element chlorine is found in plants as the
vates many enzymes involved in respiration and photo- chloride ion (Cl–). It is required for the water-splitting reac-
synthesis. The first observable symptom of potassium defi- tion of photosynthesis through which oxygen is produced
ciency is mottled or marginal chlorosis, which then (see Chapter 7) (Clarke and Eaton-Rye 2000). In addition,
develops into necrosis primarily at the leaf tips, at the mar- chlorine may be required for cell division in both leaves
gins, and between veins. In many monocots, these necrotic and roots (Harling et al. 1997). Plants deficient in chlorine
lesions may initially form at the leaf tips and margins and develop wilting of the leaf tips followed by general leaf
then extend toward the leaf base. chlorosis and necrosis. The leaves may also exhibit reduced
Because potassium can be mobilized to the younger growth. Eventually, the leaves may take on a bronzelike
leaves, these symptoms appear initially on the more color (“bronzing”). Roots of chlorine-deficient plants may
mature leaves toward the base of the plant. The leaves may appear stunted and thickened near the root tips.
also curl and crinkle. The stems of potassium-deficient Chloride ions are very soluble and generally available
plants may be slender and weak, with abnormally short in soils because seawater is swept into the air by wind and
internodal regions. In potassium-deficient corn, the roots is delivered to soil when it rains. Therefore, chlorine defi-
may have an increased susceptibility to root-rotting fungi ciency is unknown in plants grown in native or agricultural
present in the soil, and this susceptibility, together with habitats. Most plants generally absorb chlorine at levels
effects on the stem, results in an increased tendency for the much higher than those required for normal functioning.
plant to be easily bent to the ground (lodging).
MANGANESE. Manganese ions (Mn2+) activate several
CALCIUM. Calcium ions (Ca2+) are used in the synthesis of enzymes in plant cells. In particular, decarboxylases and
new cell walls, particularly the middle lamellae that sepa- dehydrogenases involved in the tricarboxylic acid (Krebs)
rate newly divided cells. Calcium is also used in the mitotic cycle are specifically activated by manganese. The best-
spindle during cell division. It is required for the normal defined function of manganese is in the photosynthetic
functioning of plant membranes and has been implicated reaction through which oxygen is produced from water
as a second messenger for various plant responses to both (Marschner 1995). The major symptom of manganese defi-
environmental and hormonal signals (Sanders et al. 1999). ciency is intervenous chlorosis associated with the devel-
In its function as a second messenger, calcium may bind to opment of small necrotic spots. This chlorosis may occur
calmodulin, a protein found in the cytosol of plant cells. on younger or older leaves, depending on plant species
The calmodulin–calcium complex regulates many meta- and growth rate.
bolic processes.
Characteristic symptoms of calcium deficiency include SODIUM. Most species utilizing the C4 and CAM pathways
necrosis of young meristematic regions, such as the tips of of carbon fixation (see Chapter 8) require sodium ions
roots or young leaves, where cell division and wall forma- (Na+). In these plants, sodium appears vital for regenerat-
tion are most rapid. Necrosis in slowly growing plants may ing phosphoenolpyruvate, the substrate for the first car-
 Mineral Nutrition 75

boxylation in the C4 and CAM pathways (Johnstone et al. Cu+ to Cu2+. An example of such an enzyme is plasto-
1988). Under sodium deficiency, these plants exhibit chloro- cyanin, which is involved in electron transfer during the
sis and necrosis, or even fail to form flowers. Many C3 light reactions of photosynthesis (Haehnel 1984). The ini-
species also benefit from exposure to low levels of sodium tial symptom of copper deficiency is the production of dark
ions. Sodium stimulates growth through enhanced cell green leaves, which may contain necrotic spots. The
expansion, and it can partly substitute for potassium as an necrotic spots appear first at the tips of the young leaves
osmotically active solute. and then extend toward the leaf base along the margins.
The leaves may also be twisted or malformed. Under
Group 4: Deficiencies in mineral nutrients that are extreme copper deficiency, leaves may abscise prematurely.
involved in redox reactions. This group of five micronu-
trients includes the metals iron, zinc, copper, nickel, and NICKEL. Urease is the only known nickel-containing
molybdenum. All of these can undergo reversible oxidations enzyme in higher plants, although nitrogen-fixing microor-
and reductions (e.g., Fe2+ ~ Fe3+) and have important roles ganisms require nickel for the enzyme that reprocesses
in electron transfer and energy transformation. They are usu- some of the hydrogen gas generated during fixation
ally found in association with larger molecules such as (hydrogen uptake hydrogenase) (see Chapter 12). Nickel-
cytochromes, chlorophyll, and proteins (usually enzymes). deficient plants accumulate urea in their leaves and, con-
sequently, show leaf tip necrosis. Plants grown in soil sel-
IRON. Iron has an important role as a component of dom, if ever, show signs of nickel deficiency because the
enzymes involved in the transfer of electrons (redox reac- amounts of nickel required are minuscule.
tions), such as cytochromes. In this role, it is reversibly oxi-
dized from Fe2+ to Fe3+ during electron transfer. As in mag- MOLYBDENUM. Molybdenum ions (Mo4+ through Mo6+)
nesium deficiency, a characteristic symptom of iron are components of several enzymes, including nitrate
deficiency is intervenous chlorosis. In contrast to magne- reductase and nitrogenase. Nitrate reductase catalyzes the
sium deficiency symptoms, these symptoms appear ini- reduction of nitrate to nitrite during its assimilation by the
tially on the younger leaves because iron cannot be readily plant cell; nitrogenase converts nitrogen gas to ammonia in
mobilized from older leaves. Under conditions of extreme nitrogen-fixing microorganisms (see Chapter 12). The first
or prolonged deficiency, the veins may also become indication of a molybdenum deficiency is general chloro-
chlorotic, causing the whole leaf to turn white. sis between veins and necrosis of the older leaves. In some
The leaves become chlorotic because iron is required for plants, such as cauliflower or broccoli, the leaves may not
the synthesis of some of the chlorophyll–protein complexes become necrotic but instead may appear twisted and sub-
in the chloroplast. The low mobility of iron is probably due sequently die (whiptail disease). Flower formation may be
to its precipitation in the older leaves as insoluble oxides or prevented, or the flowers may abscise prematurely.
phosphates or to the formation of complexes with phyto- Because molybdenum is involved with both nitrate
ferritin, an iron-binding protein found in the leaf and other assimilation and nitrogen fixation, a molybdenum defi-
plant parts (Oh et al. 1996). The precipitation of iron dimin- ciency may bring about a nitrogen deficiency if the nitrogen
ishes subsequent mobilization of the metal into the phloem source is primarily nitrate or if the plant depends on sym-
for long-distance translocation. biotic nitrogen fixation. Although plants require only small
amounts of molybdenum, some soils supply inadequate
ZINC. Many enzymes require zinc ions (Zn2+) for their levels. Small additions of molybdenum to such soils can
activity, and zinc may be required for chlorophyll biosyn- greatly enhance crop or forage growth at negligible cost.
thesis in some plants. Zinc deficiency is characterized by a
reduction in internodal growth, and as a result plants dis- Analysis of Plant Tissues Reveals
play a rosette habit of growth in which the leaves form a Mineral Deficiencies
circular cluster radiating at or close to the ground. The Requirements for mineral elements change during the
leaves may also be small and distorted, with leaf margins growth and development of a plant. In crop plants, nutri-
having a puckered appearance. These symptoms may ent levels at certain stages of growth influence the yield of
result from loss of the capacity to produce sufficient the economically important tissues (tuber, grain, and so
amounts of the auxin indoleacetic acid. In some species on). To optimize yields, farmers use analyses of nutrient
(corn, sorghum, beans), the older leaves may become inter- levels in soil and in plant tissue to determine fertilizer
venously chlorotic and then develop white necrotic spots. schedules.
This chlorosis may be an expression of a zinc requirement Soil analysis is the chemical determination of the nutri-
for chlorophyll biosynthesis. ent content in a soil sample from the root zone. As dis-
cussed later in the chapter, both the chemistry and the biol-
COPPER. Like iron, copper is associated with enzymes ogy of soils are complex, and the results of soil analyses
involved in redox reactions being reversibly oxidized from vary with sampling methods, storage conditions for the
76 Chapter 5

samples, and nutrient extraction techniques. Perhaps more adequate amounts except the nutrient under consideration.
important is that a particular soil analysis reflects the lev- At the start of the experiment, the limiting nutrient is
els of nutrients potentially available to the plant roots from added in increasing concentrations to different sets of
the soil, but soil analysis does not tell us how much of a plants, and the concentrations of the nutrient in specific tis-
particular mineral nutrient the plant actually needs or is sues are correlated with a particular measure of growth or
able to absorb. This additional information is best deter- yield. Several curves are established for each element, one
mined by plant tissue analysis. for each tissue and tissue age.
Proper use of plant tissue analysis requires an under- Because agricultural soils are often limited in the ele-
standing of the relationship between plant growth (or ments nitrogen, phosphorus, and potassium, many farm-
yield) and the mineral concentration of plant tissue sam- ers routinely use, at a minimum, curves for these elements.
ples (Bouma 1983). As the data plot in Figure 5.3 shows, If a nutrient deficiency is suspected, steps are taken to cor-
when the nutrient concentration in a tissue sample is low, rect the deficiency before it reduces growth or yield. Plant
growth is reduced. In this deficiency zone of the curve, an analysis has proven useful in establishing fertilizer sched-
increase in nutrient availability is directly related to an ules that sustain yields and ensure the food quality of
increase in growth or yield. As the nutrient availability con- many crops.
tinues to increase, a point is reached at which further addi-
tion of nutrients is no longer related to increases in growth
or yield but is reflected in increased tissue concentrations.
TREATING NUTRITIONAL DEFICIENCIES
This region of the curve is often called the adequate zone. Many traditional and subsistence farming practices pro-
The transition between the deficiency and adequate mote the recycling of mineral elements. Crop plants absorb
zones of the curve reveals the critical concentration of the the nutrients from the soil, humans and animals consume
nutrient (see Figure 5.3), which may be defined as the min- locally grown crops, and crop residues and manure from
imum tissue content of the nutrient that is correlated with humans and animals return the nutrients to the soil. The
maximal growth or yield. As the nutrient concentration of main losses of nutrients from such agricultural systems
the tissue increases beyond the adequate zone, growth or ensue from leaching that carries dissolved ions away with
yield declines because of toxicity (this is the toxic zone). drainage water. In acid soils, leaching may be decreased by
To evaluate the relationship between growth and tissue the addition of lime—a mix of CaO, CaCO3, and
nutrient concentration, researchers grow plants in soil or Ca(OH)2—to make the soil more alkaline because many
nutrient solution in which all the nutrients are present in mineral elements form less soluble compounds when the
pH is higher than 6 (Figure 5.4).
In the high-production agricultural systems of industrial
countries, the unidirectional removal of nutrients from the
soil to the crop can become significant because a large por-
Deficiency Adequate zone Toxic
tion of crop biomass leaves the area of cultivation. Plants
(percent of maximum)

zone zone
100 synthesize all their components from basic inorganic sub-
stances and sunlight, so it is important to restore these lost
Growth or yield

nutrients to the soil through the addition of fertilizers.

50 Crop Yields Can Be Improved by

Addition of Fertilizers
Most chemical fertilizers contain inorganic salts of the
macronutrients nitrogen, phosphorus, and potassium (see
0 Critical concentration Table 5.1). Fertilizers that contain only one of these three
nutrients are termed straight fertilizers. Some examples of
Concentration of nutrient in tissue
(mmol/g dry weight) straight fertilizers are superphosphate, ammonium nitrate,
and muriate of potash (a source of potassium). Fertilizers
FIGURE 5.3 Relationship between yield (or growth) and the that contain two or more mineral nutrients are called com-
nutrient content of the plant tissue. The yield parameter
may be expressed in terms of shoot dry weight or height.
pound fertilizers or mixed fertilizers, and the numbers on
Three zones—deficiency, adequate, and toxic—are indi- the package label, such as 10-14-10, refer to the effective per-
cated on the graph. To yield data of this type, plants are centages of N, P2O5, and K2O, respectively, in the fertilizer.
grown under conditions in which the concentration of one With long-term agricultural production, consumption
essential nutrient is varied while all others are in adequate of micronutrients can reach a point at which they, too, must
supply. The effect of varying the concentration of this nutri-
ent during plant growth is reflected in the growth or yield.
be added to the soil as fertilizers. Adding micronutrients to
The critical concentration for that nutrient is the concentra- the soil may also be necessary to correct a preexisting defi-
tion below which yield or growth is reduced. ciency. For example, some soils in the United States are
 Mineral Nutrition 77

water and oxygen availability, and the type and number of

Nitrogen microorganisms present in the soil.
As a consequence, the rate of mineralization is highly
Phosphorus variable, and nutrients from organic residues become avail-
able to plants over periods that range from days to months
Potassium to years. The slow rate of mineralization hinders efficient
fertilizer use, so farms that rely solely on organic fertilizers
Sulfur may require the addition of substantially more nitrogen or
phosphorus and suffer even higher nutrient losses than
Calcium farms that use chemical fertilizers. Residues from organic
fertilizers do improve the physical structure of most soils,
Magnesium enhancing water retention during drought and increasing
drainage in wet weather.
Iron
Some Mineral Nutrients Can Be
Manganese
Absorbed by Leaves
In addition to nutrients being added to the soil as fertiliz-
Boron
ers, some mineral nutrients can be applied to the leaves as
sprays, in a process known as foliar application, and the
Copper leaves can absorb the applied nutrients. In some cases, this
method can have agronomic advantages over the applica-
tion of nutrients to the soil. Foliar application can reduce
Zinc
the lag time between application and uptake by the plant,
which could be important during a phase of rapid growth.
Molybdenum
It can also circumvent the problem of restricted uptake of
a nutrient from the soil. For example, foliar application of
4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 8.0 8.5 9.0
mineral nutrients such as iron, manganese, and copper
pH
may be more efficient than application through the soil,
Acid Neutral Alkaline
where they are adsorbed on soil particles and hence are less
FIGURE 5.4 Influence of soil pH on the availability of nutri- available to the root system.
ent elements in organic soils. The width of the shaded areas Nutrient uptake by plant leaves is most effective when
indicates the degree of nutrient availability to the plant the nutrient solution remains on the leaf as a thin film
root. All of these nutrients are available in the pH range of
5.5 to 6.5. (From Lucas and Davis 1961.)
(Mengel and Kirkby 1987). Production of a thin film often
requires that the nutrient solutions be supplemented with
surfactant chemicals, such as the detergent Tween 80, that
reduce surface tension. Nutrient movement into the plant
deficient in boron, copper, zinc, manganese, molybdenum, seems to involve diffusion through the cuticle and uptake
or iron (Mengel and Kirkby 1987) and can benefit from by leaf cells. Although uptake through the stomatal pore
nutrient supplementation. could provide a pathway into the leaf, the architecture of
Chemicals may also be applied to the soil to modify soil the pore (see Figures 4.13 and 4.14) largely prevents liquid
pH. As Figure 5.4 shows, soil pH affects the availability of all penetration (Ziegler 1987).
mineral nutrients. Addition of lime, as mentioned previ- For foliar nutrient application to be successful, damage
ously, can raise the pH of acidic soils; addition of elemental to the leaves must be minimized. If foliar sprays are
sulfur can lower the pH of alkaline soils. In the latter case, applied on a hot day, when evaporation is high, salts may
microorganisms absorb the sulfur and subsequently release accumulate on the leaf surface and cause burning or
sulfate and hydrogen ions that acidify the soil. scorching. Spraying on cool days or in the evening helps to
Organic fertilizers, in contrast to chemical fertilizers, alleviate this problem. Addition of lime to the spray dimin-
originate from the residues of plant or animal life or from ishes the solubility of many nutrients and limits toxicity.
natural rock deposits. Plant and animal residues contain Foliar application has proved economically successful
many of the nutrient elements in the form of organic com- mainly with tree crops and vines such as grapes, but it is
pounds. Before crop plants can acquire the nutrient ele- also used with cereals. Nutrients applied to the leaves
ments from these residues, the organic compounds must could save an orchard or vineyard when soil-applied nutri-
be broken down, usually by the action of soil microorgan- ents would be too slow to correct a deficiency. In wheat,
isms through a process called mineralization. Mineraliza- nitrogen applied to the leaves during the later stages of
tion depends on many factors, including temperature, growth enhances the protein content of seeds.
78 Chapter 5

• Silt has particles between 0.002 and 0.02 mm.

SOIL, ROOTS, AND MICROBES
• Clay has particles smaller than 0.002 mm (see Table
The soil is a complex physical, chemical, and biological
4.1).
substrate. It is a heterogeneous material containing solid,
liquid, and gaseous phases (see Chapter 4). All of these The silicate-containing clay materials are further divided
phases interact with mineral elements. The inorganic par- into three major groups—kaolinite, illite, and montmoril-
ticles of the solid phase provide a reservoir of potassium, lonite—based on differences in their structure and physi-
calcium, magnesium, and iron. Also associated with this cal properties (Table 5.5). The kaolinite group is generally
solid phase are organic compounds containing nitrogen, found in well-weathered soils; the montmorillonite and
phosphorus, and sulfur, among other elements. The liquid illite groups are found in less weathered soils.
phase of the soil constitutes the soil solution, which con- Mineral cations such as ammonium (NH4+) and potas-
tains dissolved mineral ions and serves as the medium for sium (K+) adsorb to the negative surface charges of inor-
ion movement to the root surface. Gases such as oxygen, ganic and organic soil particles. This cation adsorption is
carbon dioxide, and nitrogen are dissolved in the soil solu- an important factor in soil fertility. Mineral cations
tion, but in roots gases are exchanged predominantly adsorbed on the surface of soil particles are not easily lost
through the air gaps between soil particles. when the soil is leached by water, and they provide a nutri-
From a biological perspective, soil constitutes a diverse ent reserve available to plant roots. Mineral nutrients
ecosystem in which plant roots and microorganisms com- adsorbed in this way can be replaced by other cations in a
pete strongly for mineral nutrients. In spite of this compe- process known as cation exchange (Figure 5.5). The degree
tition, roots and microorganisms can form alliances for to which a soil can adsorb and exchange ions is termed its
their mutual benefit (symbioses, singular symbiosis). In this cation exchange capacity (CEC) and is highly dependent on
section we will discuss the importance of soil properties, the soil type. A soil with higher cation exchange capacity
root structure, and mycorrhizal symbiotic relationships to generally has a larger reserve of mineral nutrients.
plant mineral nutrition. Chapter 12 addresses symbiotic Mineral anions such as nitrate (NO3–) and chloride (Cl–)
relationships with nitrogen-fixing bacteria. tend to be repelled by the negative charge on the surface of
soil particles and remain dissolved in the soil solution.
Negatively Charged Soil Particles Affect the Thus the anion exchange capacity of most agricultural soils
Adsorption of Mineral Nutrients is small compared to the cation exchange capacity. Among
Soil particles, both inorganic and organic, have predomi- anions, nitrate remains mobile in the soil solution, where it
nantly negative charges on their surfaces. Many inorganic is susceptible to leaching by water moving through the soil.
soil particles are crystal lattices that are tetrahedral arrange- Phosphate ions (H2PO2–) may bind to soil particles con-
ments of the cationic forms of aluminum and silicon (Al3+ taining aluminum or iron because the positively charged
and Si4+) bound to oxygen atoms, thus forming aluminates iron and aluminum ions (Fe2+, Fe3+, and Al3+) have
and silicates. When cations of lesser charge replace Al3+ and hydroxyl (OH–) groups that exchange with phosphate. As
Si4+, inorganic soil particles become negatively charged. a result, phosphate can be tightly bound, and its mobility
Organic soil particles originate from the products of the and availability in soil can limit plant growth.
microbial decomposition of dead plants, animals, and Sulfate (SO42–) in the presence of calcium (Ca2+) forms
microorganisms. The negative surface charges of organic gypsum (CaSO4). Gypsum is only slightly soluble, but it
particles result from the dissociation of hydrogen ions from releases sufficient sulfate to support plant growth. Most
the carboxylic acid and phe-
nolic groups present in this
component of the soil. Most TABLE 5.5
of the world’s soil particles,
Comparison of properties of three major types of silicate clays found in the soil
however, are inorganic. Type of clay
Inorganic soils are catego-
Property Montmorillonite Illite Kaolinite
rized by particle size:
Size (µm) 0.01–1.0 0.1–2.0 0.1–5.0
• Gravel has particles
larger than 2 mm. Shape Irregular flakes Irregular flakes Hexagonal crystals
Cohesion High Medium Low
• Coarse sand has particles
between 0.2 and 2 mm. Water-swelling capacity High Medium Low

• Fine sand has particles Cation exchange capacity 80–100 15–40 3–15
between 0.02 and (milliequivalents 100 g−1)
0.2 mm. Source: After Brady 1974.
 Mineral Nutrition 79

exchange complex in a soil. Leaching then may remove

K+ K+ these ions from the upper soil layers, leaving a more acid
Soil particle K+ soil. By contrast, the weathering of rock in arid regions
K+ releases K+, Mg2+, Ca2+, and Mn2+ to the soil, but because
K+ – H+ of the low rainfall, these ions do not leach from the upper
K+
– soil layers, and the soil remains alkaline.
H+
Ca2+ Ca2+ – Excess Minerals in the Soil Limit Plant Growth
When excess minerals are present in the soil, the soil is said
– Mg2+ –
K+ to be saline, and plant growth may be restricted if these min-
Ca2+ – eral ions reach levels that limit water availability or exceed
–
–
– the adequate zone for a particular nutrient (see Chapter 25).
Ca2+ Sodium chloride and sodium sulfate are the most common
Ca2+
Ca2+ salts in saline soils. Excess minerals in soils can be a major
problem in arid and semiarid regions because rainfall is
insufficient to leach the mineral ions from the soil layers near
FIGURE 5.5 The principle of cation exchange on the surface the surface. Irrigated agriculture fosters soil salinization if
of a soil particle. Cations are bound to the surface of soil
particles because the surface is negatively charged. insufficient water is applied to leach the salt below the root-
Addition of a cation such as potassium (K+) can displace ing zone. Irrigation water can contain 100 to 1000 g of min-
another cation such as calcium (Ca2+) from its binding on erals per cubic meter. An average crop requires about 4000
the surface of the soil particle and make it available for m3 of water per acre. Consequently, 400 to 4000 kg of min-
uptake by the root. erals may be added to the soil per crop (Marschner 1995).
In saline soil, plants encounter salt stress. Whereas
many plants are affected adversely by the presence of rel-
nonacid soils contain substantial amounts of calcium; con- atively low levels of salt, other plants can survive high lev-
sequently, sulfate mobility in these soils is low, so sulfate is els (salt-tolerant plants) or even thrive (halophytes) under
not highly susceptible to leaching. such conditions. The mechanisms by which plants tolerate
salinity are complex (see Chapter 25), involving molecular
Soil pH Affects Nutrient Availability, Soil Microbes, synthesis, enzyme induction, and membrane transport. In
and Root Growth some species, excess minerals are not taken up; in others,
Hydrogen ion concentration (pH) is an important property minerals are taken up but excreted from the plant by salt
of soils because it affects the growth of plant roots and soil glands associated with the leaves. To prevent toxic buildup
microorganisms. Root growth is generally favored in of mineral ions in the cytosol, many plants may sequester
slightly acidic soils, at pH values between 5.5 and 6.5. them in the vacuole (Stewart and Ahmad 1983). Efforts are
Fungi generally predominate in acidic soils; bacteria under way to bestow salt tolerance on salt-sensitive crop
become more prevalent in alkaline soils. Soil pH deter- species using both classic plant breeding and molecular
mines the availability of soil nutrients (see Figure 5.4). biology (Hasegawa et al. 2000).
Acidity promotes the weathering of rocks that releases K+, Another important problem with excess minerals is the
Mg2+, Ca2+, and Mn2+ and increases the solubility of car- accumulation of heavy metals in the soil, which can cause
bonates, sulfates, and phosphates. Increasing the solubility severe toxicity in plants as well as humans (see Web Essay
of nutrients facilitates their availability to roots. 5.1). Heavy metals include zinc, copper, cobalt, nickel, mer-
Major factors that lower the soil pH are the decomposi- cury, lead, cadmium, silver, and chromium (Berry and Wal-
tion of organic matter and the amount of rainfall. Carbon lace 1981).
dioxide is produced as a result of the decomposition of
organic material and equilibrates with soil water in the fol- Plants Develop Extensive Root Systems
lowing reaction: The ability of plants to obtain both water and mineral
nutrients from the soil is related to their capacity to develop
CO2 + H2O ~ H+ + HCO3 –
an extensive root system. In the late 1930s, H. J. Dittmer
This reaction releases hydrogen ions (H+), lowering the pH examined the root system of a single winter rye plant after
of the soil. Microbial decomposition of organic material 16 weeks of growth and estimated that the plant had 13 ×
also produces ammonia and hydrogen sulfide that can be 106 primary and lateral root axes, extending more than 500
oxidized in the soil to form the strong acids nitric acid km in length and providing 200 m2 of surface area (Dittmer
(HNO3) and sulfuric acid (H2SO4), respectively. Hydrogen 1937). This plant also had more than 1010 root hairs, pro-
ions also displace K+, Mg2+, Ca2+, and Mn2+ from the cation viding another 300 m2 of surface area.
80 Chapter 5

In the desert, the roots of mesquite (genus Prosopis) may (A) Dry soil (B) Irrigated soil
extend down more than 50 m to reach groundwater. Annual
crop plants have roots that usually grow between 0.1 and
2.0 m in depth and extend laterally to distances of 0.3 to 1.0
m. In orchards, the major root systems of trees planted 1 m
apart reach a total length of 12 to 18 km per tree. The annual
production of roots in natural ecosystems may easily sur-
pass that of shoots, so in many respects, the aboveground
portions of a plant represent only “the tip of an iceberg.”
Plant roots may grow continuously throughout the year.
Their proliferation, however, depends on the availability of
water and minerals in the immediate microenvironment
surrounding the root, the so-called rhizosphere. If the rhi-
zosphere is poor in nutrients or too dry, root growth is
slow. As rhizosphere conditions improve, root growth
increases. If fertilization and irrigation provide abundant
30 cm
nutrients and water, root growth may not keep pace with
shoot growth. Plant growth under such conditions
becomes carbohydrate limited, and a relatively small root FIGURE 5.6 Fibrous root systems of wheat (a monocot). (A)
system meets the nutrient needs of the whole plant (Bloom The root system of a mature (3-month-old) wheat plant
et al. 1993). Roots growing below the soil surface are stud- growing in dry soil. (B) The root system of a wheat plant
ied by special techniques (see Web Topic 5.2). growing in irrigated soil. It is apparent that the morphol-
ogy of the root system is affected by the amount of water
Root Systems Differ in Form but Are Based on present in the soil. In a fibrous root system, the primary
root axes are no longer distinguishable. (After Weaver
Common Structures 1926.)
The form of the root system differs greatly among plant
species. In monocots, root development starts with the
emergence of three to six primary (or seminal) root axes
from the germinating seed. With further growth, the plant that it lubricates the penetration of the root through the
extends new adventitious roots, called nodal roots or brace soil, protects the root apex from desiccation, promotes the
roots. Over time, the primary and nodal root axes grow and transfer of nutrients to the root, or affects the interaction
branch extensively to form a complex fibrous root system between roots and soil microorganisms (Russell 1977). The
(Figure 5.6). In fibrous root systems, all the roots generally root cap is central to the perception of gravity, the signal
have the same diameter (except where environmental con- that directs the growth of roots downward. This process is
ditions or pathogenic interactions modify the root struc- termed the gravitropic response (see Chapter 19).
ture), so it is difficult to distinguish a main root axis. Cell division at the root apex proper is relatively slow;
In contrast to monocots, dicots develop root systems thus this region is called the quiescent center. After a few
with a main single root axis, called a taproot, which may generations of slow cell divisions, root cells displaced from
thicken as a result of secondary cambial activity. From this the apex by about 0.1 mm begin to divide more rapidly.
main root axis, lateral roots develop to form an extensively Cell division again tapers off at about 0.4 mm from the
branched root system (Figure 5.7). apex, and the cells expand equally in all directions.
The development of the root system in both monocots The elongation zone begins 0.7 to 1.5 mm from the apex
and dicots depends on the activity of the root apical meri- (see Figure 5.8). In this zone, cells elongate rapidly and
stem and the production of lateral root meristems. Figure undergo a final round of divisions to produce a central ring
5.8 shows a generalized diagram of the apical region of a of cells called the endodermis. The walls of this endoder-
plant root and identifies the three zones of activity: meri- mal cell layer become thickened, and suberin (see Chapter
stematic, elongation, and maturation. 13) deposited on the radial walls forms the Casparian strip,
In the meristematic zone, cells divide both in the direc- a hydrophobic structure that prevents the apoplastic move-
tion of the root base to form cells that will differentiate into ment of water or solutes across the root (see Figure 4.3).
the tissues of the functional root and in the direction of the The endodermis divides the root into two regions: the cor-
root apex to form the root cap. The root cap protects the tex toward the outside and the stele toward the inside. The
delicate meristematic cells as the root moves through the stele contains the vascular elements of the root: the
soil. It also secretes a gelatinous material called mucigel, phloem, which transports metabolites from the shoot to the
which commonly surrounds the root tip. The precise func- root, and the xylem, which transports water and solutes to
tion of the mucigel is uncertain, but it has been suggested the shoot.
 Mineral Nutrition 81

(Bret-Harte and Silk 1994). The low rates of cell division in

the quiescent center may result from the fact that insuffi-
cient carbohydrates reach this centrally located region or
that this area is kept in an oxidized state (see Web Essay
5.2).
Root hairs, with their large surface area for absorption
of water and solutes, first appear in the maturation zone
(see Figure 5.8), and it is here that the xylem develops the
capacity to translocate substantial quantities of water and
solutes to the shoot.

Root hair

Maturation zone

Cortex

Xylem
Stele
Phloem

Endodermis
Elongation zone

with Casparian
30 cm strip
Sugar beet Alfalfa
Epidermis

FIGURE 5.7 Taproot system of two adequately watered

dicots: sugar beet and alfalfa. The sugar beet root system is Region of
typical of 5 months of growth; the alfalfa root system is typ- rapid cell
ical of 2 years of growth. In both dicots, the root system division
Meristematic

shows a major vertical root axis. In the case of sugar beet,

the upper portion of the taproot system is thickened
zone

Quiescent
because of its function as storage tissue. (After Weaver center (few
1926.) cell divisions)

Root cap

Phloem develops more rapidly than xylem, attesting to Mucigel

the fact that phloem function is critical near the root apex. sheath
Large quantities of carbohydrates must flow through the
phloem to the growing apical zones in order to support cell
Apex
division and elongation. Carbohydrates provide rapidly
growing cells with an energy source and with the carbon FIGURE 5.8 Diagrammatic longitudinal section of the apical
skeletons required to synthesize organic compounds. Six- region of the root. The meristematic cells are located near
carbon sugars (hexoses) also function as osmotically active the tip of the root. These cells generate the root cap and the
upper tissues of the root. In the elongation zone, cells dif-
solutes in the root tissue. At the root apex, where the
ferentiate to produce xylem, phloem, and cortex. Root
phloem is not yet developed, carbohydrate movement hairs, formed in epidermal cells, first appear in the matura-
depends on symplastic diffusion and is relatively slow tion zone.
82 Chapter 5

Different Areas of the Root Absorb of nutrients down their concentration gradient and bulk
Different Mineral Ions flow resulting from transpiration can increase nutrient
The precise point of entry of minerals into the root system availability at the root surface.
has been a topic of considerable interest. Some researchers When absorption of nutrients by the roots is high and
have claimed that nutrients are absorbed only at the apical the nutrient concentration in the soil is low, bulk flow can
regions of the root axes or branches (Bar-Yosef et al. 1972); supply only a small fraction of the total nutrient require-
others claim that nutrients are absorbed over the entire root ment (Mengel and Kirkby 1987). Under these conditions,
surface (Nye and Tinker 1977). Experimental evidence sup- diffusion rates limit the movement of nutrients to the root
ports both possibilities, depending on the plant species and surface. When diffusion is too slow to maintain high nutri-
the nutrient being investigated: ent concentrations near the root, a nutrient depletion zone
• Root absorption of calcium in barley appears to be forms adjacent to the root surface (Figure 5.9). This zone
restricted to the apical region. extends from about 0.2 to 2.0 mm from the root surface,
depending on the mobility of the nutrient in the soil.
• Iron may be taken up either at the apical region, as in The formation of a depletion zone tells us something
barley (Clarkson 1985), or over the entire root sur- important about mineral nutrition: Because roots deplete
face, as in corn (Kashirad et al. 1973). the mineral supply in the rhizosphere, their effectiveness
• Potassium, nitrate, ammonium, and phosphate can in mining minerals from the soil is determined not only by
be absorbed freely at all locations of the root surface the rate at which they can remove nutrients from the soil
(Clarkson 1985), but in corn the elongation zone has solution, but by their continuous growth. Without growth,
the maximum rates of potassium accumulation roots would rapidly deplete the soil adjacent to their surface.
(Sharp et al. 1990) and nitrate absorption (Taylor and Optimal nutrient acquisition therefore depends both on the capac-
Bloom 1998). ity for nutrient uptake and on the ability of the root system to
grow into fresh soil.
• In corn and rice, the root apex absorbs ammonium
more rapidly than the elongation zone does (Colmer
Mycorrhizal Fungi Facilitate Nutrient
and Bloom 1998).
Uptake by Roots
• In several species, root hairs are the most active in Our discussion thus far has centered on the direct acqui-
phosphate absorption (Fohse et al. 1991). sition of mineral elements by the root, but this process may
The high rates of nutrient absorption in the apical root be modified by the association of mycorrhizal fungi with
zones result from the strong demand for nutrients in these the root system. Mycorrhizae (singular mycorrhiza, from the
tissues and the relatively high nutrient availability in the Greek words for “fungus” and “root”) are not unusual; in
soil surrounding them. For example, cell elongation fact, they are widespread under natural conditions. Much
depends on the accumulation of solutes such as potassium, of the world’s vegetation appears to have roots associated
chloride, and nitrate to increase the osmotic pressure
within the cell (see Chapter 15). Ammonium is the pre-
ferred nitrogen source to support cell division in the meri-
stem because meristematic tissues are often carbohydrate High nutrient level
limited, and the assimilation of ammonium consumes less
Nutrient concentration

energy than that of nitrate (see Chapter 12). The root apex
in the soil solution

and root hairs grow into fresh soil, where nutrients have
not yet been depleted. Depletion
Within the soil, nutrients can move to the root surface zones
both by bulk flow and by diffusion (see Chapter 3). In bulk Low nutrient level
flow, nutrients are carried by water moving through the
soil toward the root. The amount of nutrient provided to
the root by bulk flow depends on the rate of water flow
through the soil toward the plant, which depends on tran-
spiration rates and on nutrient levels in the soil solution.
When both the rate of water flow and the concentrations of Distance from the root surface
nutrients in the soil solution are high, bulk flow can play FIGURE 5.9 Formation of a nutrient depletion zone in the
an important role in nutrient supply. region of the soil adjacent to the plant root. A nutrient
In diffusion, mineral nutrients move from a region of depletion zone forms when the rate of nutrient uptake by
higher concentration to a region of lower concentration. the cells of the root exceeds the rate of replacement of the
nutrient by diffusion in the soil solution. This depletion
Nutrient uptake by the roots lowers the concentration of causes a localized decrease in the nutrient concentration in
nutrients at the root surface, generating concentration gra- the area adjacent to the root surface. (After Mengel and
dients in the soil solution surrounding the root. Diffusion Kirkby 1987.)
 Mineral Nutrition 83

with mycorrhizal fungi: 83% of dicots, 79% of monocots, mass is comparable to that of the roots themselves. The
and all gymnosperms regularly form mycorrhizal associa- fungal mycelium also extends into the soil, away from this
tions (Wilcox 1991). compact mantle, where it forms individual hyphae or
On the other hand, plants from the families Cruciferae strands containing fruiting bodies.
(cabbage), Chenopodiaceae (spinach), and Proteaceae The capacity of the root system to absorb nutrients is
(macadamia nuts), as well as aquatic plants, rarely if ever improved by the presence of external fungal hyphae that
have mycorrhizae. Mycorrhizae are absent from roots in are much finer than plant roots and can reach beyond the
very dry, saline, or flooded soils, or where soil fertility is areas of nutrient-depleted soil near the roots (Clarkson
extreme, either high or low. In particular, plants grown 1985). Ectotrophic mycorrhizal fungi infect exclusively tree
under hydroponics and young, rapidly growing crop species, including gymnosperms and woody angiosperms.
plants seldom have mycorrhizae. Unlike the ectotrophic mycorrhizal fungi, vesicular-
Mycorrhizal fungi are composed of fine, tubular fila- arbuscular mycorrhizal fungi do not produce a compact
ments called hyphae (singular hypha). The mass of hyphae mantle of fungal mycelium around the root. Instead, the
that forms the body of the fungus is called the mycelium hyphae grow in a less dense arrangement, both within the
(plural mycelia). There are two major classes of mycorrhizal root itself and extending outward from the root into the
fungi: ectotrophic mycorrhizae and vesicular-arbuscular surrounding soil (Figure 5.11). After entering the root
mycorrhizae (Smith et al. 1997). Minor classes of mycor- through either the epidermis or a root hair, the hyphae not
rhizal fungi include the ericaceous and orchidaceous myc- only extend through the regions between cells but also pen-
orrhizae, which may have limited importance in terms of etrate individual cells of the cortex. Within the cells, the
mineral nutrient uptake. hyphae can form oval structures called vesicles and
Ectotrophic mycorrhizal fungi typically show a thick branched structures called arbuscules. The arbuscules
sheath, or “mantle,” of fungal mycelium around the roots, appear to be sites of nutrient transfer between the fungus
and some of the mycelium penetrates between the cortical and the host plant.
cells (Figure 5.10). The cortical cells themselves are not pen-
etrated by the fungal hyphae but instead are surrounded
by a network of hyphae called the Hartig net. Often the
amount of fungal mycelium is so extensive that its total

Reproductive
chlamydospore

Epidermis Epidermis

Xylem
Arbuscule
Phloem

Endodermis
Cortex
Hartig net
Vesicle

Fungal Root hair

sheath

External Cortex
mycelium
Root

FIGURE 5.11 Association of vesicular-arbuscular mycor-

rhizal fungi with a section of a plant root. The fungal
100 mm hyphae grow into the intercellular wall spaces of the cortex
FIGURE 5.10 Root infected with ectotrophic mycorrhizal and penetrate individual cortical cells. As they extend into
fungi. In the infected root, the fungal hyphae surround the the cell, they do not break the plasma membrane or the
root to produce a dense fungal sheath and penetrate the tonoplast of the host cell. Instead, the hypha is surrounded
intercellular spaces of the cortex to form the Hartig net. The by these membranes and forms structures known as arbus-
total mass of fungal hyphae may be comparable to the root cules, which participate in nutrient ion exchange between
mass itself. (From Rovira et al. 1983.) the host plant and the fungus. (From Mauseth 1988.)
84 Chapter 5

Outside the root, the external mycelium can extend sev- from carbon dioxide, water, and mineral elements. Studies
eral centimeters away from the root and may contain of plant nutrition have shown that specific mineral ele-
spore-bearing structures. Unlike the ectotrophic mycor- ments are essential for plant life. These elements are clas-
rhizae, vesicular-arbuscular mycorrhizae make up only a sified as macronutrients or micronutrients, depending on
small mass of fungal material, which is unlikely to exceed the relative amounts found in plant tissue.
10% of the root weight. Vesicular-arbuscular mycorrhizae Certain visual symptoms are diagnostic for deficiencies
are found in association with the roots of most species of in specific nutrients in higher plants. Nutritional disorders
herbaceous angiosperms (Smith et al. 1997). occur because nutrients have key roles in plant metabolism.
The association of vesicular-arbuscular mycorrhizae They serve as components of organic compounds, in
with plant roots facilitates the uptake of phosphorus and energy storage, in plant structures, as enzyme cofactors,
trace metals such as zinc and copper. By extending beyond and in electron transfer reactions. Mineral nutrition can be
the depletion zone for phosphorus around the root, the studied through the use of hydroponics or aeroponics,
external mycelium improves phosphorus absorption. Cal- which allow the characterization of specific nutrient
culations show that a root associated with mycorrhizal requirements. Soil and plant tissue analysis can provide
fungi can transport phosphate at a rate more than four information on the nutritional status of the plant–soil sys-
times higher than that of a root not associated with myc- tem and can suggest corrective actions to avoid deficien-
orrhizae (Nye and Tinker 1977). The external mycelium of cies or toxicities.
the ectotrophic mycorrhizae can also absorb phosphate and When crop plants are grown under modern high-pro-
make it available to the plant. In addition, it has been sug- duction conditions, substantial amounts of nutrients are
gested that ectotrophic mycorrhizae proliferate in the removed from the soil. To prevent the development of defi-
organic litter of the soil and hydrolyze organic phosphorus ciencies, nutrients can be added back to the soil in the form
for transfer to the root (Smith et al. 1997). of fertilizers. Fertilizers that provide nutrients in inorganic
forms are called chemical fertilizers; those that derive from
Nutrients Move from the Mycorrhizal Fungi plant or animal residues are considered organic fertilizers.
to the Root Cells In both cases, plants absorb the nutrients primarily as inor-
Little is known about the mechanism by which the mineral ganic ions. Most fertilizers are applied to the soil, but some
nutrients absorbed by mycorrhizal fungi are transferred to are sprayed on leaves.
the cells of plant roots. With ectotrophic mycorrhizae, inor- The soil is a complex substrate—physically, chemically,
ganic phosphate may simply diffuse from the hyphae in and biologically. The size of soil particles and the cation
the Hartig net and be absorbed by the root cortical cells. exchange capacity of the soil determine the extent to which
With vesicular-arbuscular mycorrhizae, the situation may a soil provides a reservoir for water and nutrients. Soil pH
be more complex. Nutrients may diffuse from intact arbus- also has a large influence on the availability of mineral ele-
cules to root cortical cells. Alternatively, because some root ments to plants.
arbuscules are continually degenerating while new ones If mineral elements, especially sodium or heavy metals,
are forming, degenerating arbuscules may release their are present in excess in the soil, plant growth may be
internal contents to the host root cells. adversely affected. Certain plants are able to tolerate excess
A key factor in the extent of mycorrhizal association mineral elements, and a few species—for example, halo-
with the plant root is the nutritional status of the host plant. phytes in the case of sodium—grow under these extreme
Moderate deficiency of a nutrient such as phosphorus conditions.
tends to promote infection, whereas plants with abundant To obtain nutrients from the soil, plants develop exten-
nutrients tend to suppress mycorrhizal infection. sive root systems. Roots have a relatively simple structure
Mycorrhizal association in well-fertilized soils may shift with radial symmetry and few differentiated cell types.
from a symbiotic relationship to a parasitic one in that the Roots continually deplete the nutrients from the immedi-
fungus still obtains carbohydrates from the host plant, but ate soil around them, and such a simple structure may per-
the host plant no longer benefits from improved nutrient mit rapid growth into fresh soil.
uptake efficiency. Under such conditions, the host plant Plant roots often form associations with mycorrhizal
may treat mycorrhizal fungi as it does other pathogens fungi. The fine hyphae of mycorrhizae extend the reach of
(Brundrett 1991; Marschner 1995). roots into the surrounding soil and facilitate the acquisition
of mineral elements, particularly those like phosphorus
that are relatively immobile in the soil. In return, plants
SUMMARY provide carbohydrates to the mycorrhizae. Plants tend to
Plants are autotrophic organisms capable of using the suppress mycorrhizal associations under conditions of high
energy from sunlight to synthesize all their components nutrient availability.
 Mineral Nutrition 85

Web Material Bret-Harte, M. S., and Silk, W. K. (1994) Nonvascular, symplasmic

diffusion of sucrose cannot satisfy the carbon demands of growth
in the primary root tip of Zea mays L. Plant Physiol. 105: 19–33.
Brundrett, M. C. (1991) Mycorrhizas in natural ecosystems. Adv. Ecol.
Web Topics Res. 21: 171–313.
5.1 Symptoms of Deficiency in Essential Minerals Clarke, S. M., and Eaton-Rye, J. J. (2000) Amino acid deletions in loop
C of the chlorophyll a-binding protein CP47 alter the chloride
Defficiency symptoms are characteristic of each requirement and/or prevent the assembly of photosystem II.
essential element and can be used as diagnostic Plant Mol. Biol. 44: 591–601.
for the defficiency. These color pictures illustrate Clarkson, D. T. (1985) Factors affecting mineral nutrient acquisition
defficiency symptoms for each essential element by plants. Annu. Rev. Plant Physiol. 36: 77–116.
in a tomato. Colmer, T. D., and Bloom, A. J. (1998) A comparison of net NH4+ and
NO3– fluxes along roots of rice and maize. Plant Cell Environ. 21:
5.2 Observing Roots below Ground 240–246.
The study of roots growing under natural condi- Cooper, A. (1979) The ABC of NFT: Nutrient Film Technique: The
tions requires means to observe roots below World’s First Method of Crop Production without a Solid Rooting
Medium. Grower Books, London.
ground. State-of-the-art techniques are described
Dittmer, H. J. (1937) A quantitative study of the roots and root hairs
in this essay. of a winter rye plant (Secale cereale). Am. J. Bot. 24: 417–420.
Epstein, E. (1972) Mineral Nutrition of Plants: Principles and Perspec-
tives. Wiley, New York.
Web Essays Epstein, E. (1999) Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:
5.1 From Meals to Metals and Back 641–664.
Evans, H. J., and Sorger, G. J. (1966) Role of mineral elements with
Heavy metal accumulation by plants is toxic. emphasis on the univalent cations. Annu. Rev. Plant Physiol. 17:
Understanding of the involved molecular 47–76.
process is helping to develop better phytoreme- Foehse, D., Claassen, N., and Jungk, A. (1991) Phosphorus efficiency
diation crops. of plants. II. Significance of root radius, root hairs and cation-
anion balance for phosphorus influx in seven plant species. Plant
5.2 Redox Control of the Root Quiescent Center Soil 132: 261–272.
The redox status of the quiescent center seems Gericke, W. F. (1937) Hydroponics—Crop production in liquid cul-
to control the cell cycle of these cells. ture media. Science 85: 177–178.
Haehnel, W. (1984) Photosynthetic electron transport in higher
plants. Annu. Rev. Plant Physiol. 35: 659–693.
Harling, H., Czaja, I., Schell, J., and Walden, R. (1997) A plant cation-
Chapter References chloride co-transporter promoting auxin-independent tobacco
protoplast division. EMBO J. 16: 5855–5866.
Arnon, D. I., and Stout, P. R. (1939) The essentiality of certain ele- Hasegawa, P. M., Bressan, R. A., Zhu, J.-K., and Bohnert, H. J. (2000)
ments in minute quantity for plants with special reference to cop- Plant cellular and molecular responses to high salinity. Annu. Rev.
per. Plant Physiol. 14: 371–375. Plant Physiol. Plant Mol. Biol. 51: 463–499.
Asher, C. J., and Edwards, D. G. (1983) Modern solution culture tech- Hepler, P. K., and Wayne, R. O. (1985) Calcium and plant develop-
niques. In Inorganic Plant Nutrition (Encyclopedia of Plant Phys- ment. Annu. Rev. Plant Physiol. 36: 397–440.
iology, New Series, Vol. 15B), A. Läuchli and R. L. Bieleski, eds., Johnstone, M., Grof, C. P. L., and Brownell, P. F. (1988) The effect of
Springer, Berlin, pp. 94–119. sodium nutrition on the pool sizes of intermediates of the C4 pho-
Bar-Yosef, B., Kafkafi, U., and Bresler, E. (1972) Uptake of phospho- tosynthetic pathway. Aust. J. Plant Physiol. 15: 749–760.
rus by plants growing under field conditions. I. Theoretical Kashirad, A., Marschner, H., and Richter, C. H. (1973) Absorption
model and experimental determination of its parameters. Soil Sci. and translocation of 59Fe from various parts of the corn plant. Z.
36: 783–800. Pflanzenernähr. Bodenk. 134: 136–147.
Berry, W. L., and Wallace, A. (1981) Toxicity: The concept and rela- Loomis, R. S., and Connor, D. J. (1992) Crop Ecology: Productivity and
tionship to the dose response curve. J. Plant Nutr. 3: 13–19. Management in Agricultural Systems. Cambridge University Press,
Bloom, A. J. (1994) Crop acquisition of ammonium and nitrate. In Cambridge.
Physiology and Determination of Crop Yield, K. J. Boote, J. M. Ben- Lucas, R. E., and Davis, J. F. (1961) Relationships between pH values
nett, T. R. Sinclair, and G. M. Paulsen, eds., Soil Science Society of of organic soils and availabilities of 12 plant nutrients. Soil Sci. 92:
America, Inc., Crop Science Society of America, Inc., Madison, 177–182.
WI, pp. 303–309. Macek, T., Mackova, M., and Kas, J. (2000) Exploitation of plants for
Bloom, A. J., Jackson, L. E., and Smart, D. R. (1993) Root growth as a the removal of organics in environmental remediation. Biotech.
function of ammonium and nitrate in the root zone. Plant Cell Adv. 18: 23–34.
Environ. 16: 199–206. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd ed. Aca-
Bouma, D. (1983) Diagnosis of mineral deficiencies using plant tests. demic Press, London.
In Inorganic Plant Nutrition (Encyclopedia of Plant Physiology, Mauseth, J. D. (1988) Plant Anatomy. Benjamin/Cummings Pub. Co.,
New Series, Vol. 15B), A. Läuchli and R. L. Bieleski, eds., Springer, Menlo Park, CA.
Berlin, pp. 120–146. Mengel, K., and Kirkby, E. A. (1987) Principles of Plant Nutrition. Inter-
Brady, N. C. (1974) The Nature and Properties of Soils, 8th ed. Macmil- national Potash Institute, Worblaufen-Bern, Switzerland.
lan, New York. Nolan, B. T. and Stoner, J. D. (2000) Nutrients in groundwater of the
center conterminous United States 1992-1995. Environ. Sci. Tech.
34: 1156–1165.
86 Chapter 5

Nye, P. H., and Tinker, P. B. (1977) Solute Movement in the Soil-Root Sievers, R. E., and Bailar, J. C., Jr. (1962) Some metal chelates of eth-
System. University of California Press, Berkeley. ylenediaminetetraacetic acid, diethylenetriaminepentaacetic acid,
Oh, S.-H., Cho, S.-W., Kwon, T.-H., and Yang, M.-S. (1996) Purifica- and triethylenetriaminehexaacetic acid. Inorganic Chem. 1:
tion and characterization of phytoferritin. J. Biochem. Mol. Biol. 29: 174–182.
540–544. Smith, S. E., Read, D. J., and Harley, J. L. (1997) Mycorrhizal Symbio-
Raven, J. A., and Smith, F. A. (1976) Nitrogen assimilation and trans- sis. Academic Press, San Diego, CA.
port in vascular land plants in relation to intracellular pH regu- Stewart, G. R., and Ahmad, I. (1983) Adaptation to salinity in
lation. New Phytol. 76: 415–431. angiosperm halophytes. In Metals and Micronutrients: Uptake and
Rovira, A. D., Bowen, C. D., and Foster, R. C. (1983) The significance Utilization by Plants, D. A. Robb and W. S. Pierpoint, eds., Acad-
of rhizosphere microflora and mycorrhizas in plant nutrition. In emic Press, New York, pp. 33–50.
Inorganic Plant Nutrition (Encyclopedia of Plant Physiology, New Taylor, A. R., and Bloom, A. J. (1998) Ammonium, nitrate and pro-
Series, Vol. 15B) A. Läuchli and R. L. Bieleskis, eds., Springer, ton fluxes along the maize root. Plant Cell Environ. 21: 1255–1263.
Berlin, pp. 61–93. Weathers, P. J., and Zobel, R. W. (1992) Aeroponics for the culture of
Russell, R. S. (1977) Plant Root Systems: Their Function and Interaction organisms, tissues, and cells. Biotech. Adv. 10: 93–115.
with the Soil. McGraw-Hill, London. Weaver, J. E. (1926) Root Development of Field Crops. McGraw-Hill,
Sanders, D., Brownlee, C., and Harper J. F. (1999) Communicating New York.
with calcium. Plant Cell 11: 691–706. Wilcox, H. E. (1991) Mycorrhizae. In Plant Roots: The Hidden Half, Y.
Sharp, R. E., Hsiao, T. C., and Silk, W. K. (1990) Growth of the maize Waisel, A. Eshel, and U. Kafkafi, eds., Marcel Dekker, New York,
primary root at low water potentials. 2. Role of growth and depo- pp. 731–765.
sition of hexose and potassium in osmotic adjustment. Plant Ziegler, H. (1987) The evolution of stomata. In Stomatal Function, E.
Physiol. 93: 1337–1346. Zeiger, G. Farquhar, and I. Cowan, eds., Stanford University
Shelp, B. J. (1993) Physiology and biochemistry of boron in plants. Press, Stanford, CA, pp. 29–57.
In Boron and Its Role in Crop Production, U. C. Gupta, ed., CRC
Press, Boca Raton, FL, pp. 53–85.